PubMed 1, Supplementary Fig. At a general level, the relative abundance of PCS annotated for CAZy families reveals that the microbiota of FGI tend to exhibit a higher relative abundance of PCS classified as GH and GT, followed by AA and CE (Fig. Article Because of the low number of protein coding sequences annotated as PL (polysaccharide lyases, PCS<100) in the FGI microbiota, these functions are not depicted. Even so, considering the diversity of lower attine ants11, it is also possible that different antspecies could host taxonomically diverse microbiota that would include different dominant taxa. 37, D233D238. Even though FGI differ regarding geographic distribution, evolutionary history, and fungal taxa maintained as crops9, marked similarities in microbiota taxonomic composition at higher hierarchical levels (e.g. (c) UPGMA-clustering estimated based on BrayCurtis distances (Boot N=10,000) using the normalized abundance of protein coding sequences taxonomically assigned at genera level. Comparing FGI to other hosts reveals a microbiota taxonomic composition that seems distinctive of attine ants fungus gardens, macrotermitine termites gut and fungus combs, galleries and gut of ambrosia and bark beetles. & Morishima, K. BlastKOALA & GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. Fungi form mutualistic associations with many types of organisms, including cyanobacteria, algae . Physiol. There are several hundred species in some dozen genera, of which Acromyrmex and Atta are the conspicuous leaf-cutters. Proc. 1, Supplementary Table S1). A similar pattern occurs in the cluster comprising the microbiota associated with the omnivorous Panchlora sp. Donaldson, G., Lee, S. & Mazmanian, S. Gut biogeography of the bacterial microbiota. Functional profile of the hosts microbiota was predicted through KEGG pathways (via KO terms) and CAZy families. They can thrive in seemingly hostile environments, such as the tundra, thanks to a most successful symbiosis with . Herbivorous insects clustered in four main groups (Fig. However, the definition does not describe the quality of the interaction. The carbohydrate-active enZymes database (CAZy): an expert resource for glycogenomics. Sequences taxonomically assigned to the most abundant bacterial genera classified by COG functional categories for the microbiota of (a) Mycocepurus goeldii and (b) Atta sexdens rubropilosa. The ant is bene . In these associations, the fungi derive photosynthetic sugars from the plants, and they assist the plant by facilitating the uptake of mineral nutrients and water. Ecol. https://doi.org/10.1371/journal.pgen.1001129 (2010). S7). Sci. Google Scholar. II) For the cluster that comprises the gut microbiota of Primates and Rodentia hosts, the most abundant CAZy-codifier members are Firmicutes (Bacilli and Clostridia), Bacteroidetes, and Gammaproteobacteria (Enterobacteria). (a) Metagenomic clustering using alignment-free k-mer based approach (k=15). designed the study and contributed to the results interpretation. Bio. CAS Such taxonomic convergence could indicate functional convergence, since similar traits may independently evolve in multiple microbial lineages that are not necessarily phylogenetically related37,38,39. IMG/M 4 version of the integrated metagenome comparative analysis system. 5) could indicate these pathways influencing the FGI microbiota lignocellulolytic activity66,67,68 as reported for other plant biomass-degrading communities53,69. Louca, S., Parfrey, L. W. & Doebeli, M. Decoupling function and taxonomy in the global ocean microbiome. Gammaproteobacteria-enriched communities of FGI codify for diverse carbohydrate-active enzymes (Fig. Potential applications of insect symbionts in biotechnology. Many ants . Microbiol. . Since the plant and the fungus are helping each other out, this is a mutualistic relationship, a type of symbiosis known as mutualism. Martiny, J. Symbiotic relationships have had an essential role in termite evolution and involve a range of intestinal microorganisms Koh, A., De Vadder, F., Kovatcheva-Datchary, P. & Bckhed, F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. 4, and Supplementary Figs. H.F. performed bioinformatics analysis and contributed to the results interpretation. 57, 21882203. Ants that farm fungus have been found in the Americas in tropical forests, deserts, and grasslands. S12); glycan pathways related to lipopolysaccharide biosynthesis (SupplementaryFig. Symbiosis It had previously been proposed that fungus-growing ants and their fungal cultivars are diffusely associated that is, the two partners are not exclusively associated with each other. Lange, L. & Grell, M. N. The prominent role of fungi and fungal enzymes in the antfungus biomass conversion symbiosis. The bacterial community from At. https://doi.org/10.1111/j.1469-8137.2007.02325.x (2008). Natl Acad. Hosts are depicted according to their phylogenetic relationship and diet (detailed in Supplementary Table S1). 3b), assigned mainly as Gammaproteobacteria (Enterobacteria and Others), Betaproteobacteria, and Alphaproteobacteria (SupplementaryFigs. https://doi.org/10.1046/j.1365-2435.2003.00718.x (2003). 6, e1001129. Google Scholar. Fungus-Growing Ants | Science https://doi.org/10.3390/f5030439 (2014). 1a). New Phytol. Next to ours, leafcutter ant society is the most complex society on earth. 72, 62046211. https://doi.org/10.1038/nrmicro.2016.94 (2016). Article Biochem. Hyodo, F. et al. Flemming, H. et al. Acad. Appl. Frontiers | Pseudonocardia Symbionts of Fungus-Growing Ants and the Chem. PubMedGoogle Scholar. Fungus-Growing Ants: A symbiotic relationship exists between an insect and a plant, involving an effective culturing technique. Annu. Exceptions to this pattern may be observed in the microbiota composition of M. goeldii fungus garden (in which Gammaproteobacteria and Bacteroidia are similarly abundant) and the microbiota of At. 60, 199214. The ants feed the fungi to . https://doi.org/10.1016/j.soilbio.2017.12.012 (2018). Fungi Symbiosis ( Read ) | Biology | CK-12 Foundation preying on competing fungi. Google Scholar. 3a). A. Sign up for the Nature Briefing newsletter what matters in science, free to your inbox daily. 3:54 Deep in the Amazon. The analyses reported here partially feature in the masters dissertation of M.O.B., particularly the data presented in Fig. Biol. 4b), a pattern that is also observed for the gut microbiota of the herbivorous Cephalotes ants, Anoplophora larvae gut, V. sinuatocollis beetles gallery, and for the omnivorous Panchlora sp. https://doi.org/10.1016/j.cbpa.2015.10.018 (2015). Google Scholar. 32, 17921797. Microbiome 5, 122. https://doi.org/10.1186/s40168-017-0340-0 (2017). Ants are eusocial insects belong to family Formicidae and live in symbiotic association with different species of the fungus. Six, D. L. Ecological and evolutionary determinants of bark beetle-fungus symbioses. Biochem. Correspondence to Ballard, R. W., Palleroni, N. J., Doudoroff, M., Stanier, R. Y. https://doi.org/10.1128/AEM.00068-13 (2013). Insect Sci. Internet Explorer). Biol. SymbiosisThe Cooperation of Life | Answers in Genesis Such perspective emphasizes the need to further investigate FGI ecosystems, not only for their potential to codify for natural products88,89 and biotechnologically important enzymes90, but also to unveil the ecological relevance of microbiota-fungal metabolic networks fundamental to FGI evolutionary success. https://doi.org/10.1128/AEM.00754-06 (2006). & Bork, P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Aylward, F. O. et al. Li, D., Liu, C., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Protein coding sequences annotated as CAZy were classified by CAZy family (GH, GT, CE, CBM, AA, and PL) using Blast2GO Pro, and these sequences were taxonomically annotated using GhostKOALA108 by searching in genus_prokaryotes and family_eukaryotes KEGG GENES database. The fungal phylogeny based on cladistic analyses of nuclear 28 S ribosomal DNA indicates that, in contrast with the monophyly of the ants, the attine fungi are polyphyletic. BMC Evol. https://doi.org/10.1071/AN17382 (2017). Rev. 3 and 4)50. Fungus garden metagenomes from M. goeldii and At. S18). The definition does not describe the quality of the interaction. Within CAZy families, the most abundant CAZy functions codified by the microbiota associated with FGI include: GH 1, GH 3, GH 13, GH 23, GH 43, GT 2, GT 4, GT 9, GT 35, GT51, CE 4, CE 9, CE11, CBM 48, CBM 50, AA 2, AA 3, AA 8 (Fig. 22, 261266. An Attina queen's daughter begins a new colony with . https://doi.org/10.1111/mec.13872 (2016). In Evolutionary biology: convergent evolution, evolution of complex traits, concepts and methods, Chapter 2, (ed. Expert Answer. Scott, J. J. et al. Genome sequence of Streptomyces griseus strain XyelbKG-1, an ambrosia beetle associated actinomycete. 4, Supplementary Figs. A.R. Heatmaps constructed based on the normalized abundance of CAZy sequences taxonomically assigned. Morrison, M., Pope, P. B., Denman, S. E. & McSweeney, C. S. Plant biomass degradation by gut microbiomes: more of the same or something new?. Figure 6.11. https://doi.org/10.1111/mec.12421(2013). Fungus-growing . https://doi.org/10.1128/AEM.00046-15 (2015). Curr. For instance, bacteria in some plant decomposer communities make nitrogen available to fungi while receiving labile carbon compounds in exchange70,71, and similar networks could be operating in the fungiculture environment26. cockroaches, the herbivorous Sirex noctilio wasp, and the fungus-growing beetle Xyleborus affinis. 1, 15005. https://doi.org/10.1038/npjbiofilms.2015.5 (2015). S1) and low class-diversity (Supplementary Fig. Symbiotic relationships between soil fungi and plants reduce N2O Ant-plants and fungi: a new threeway symbiosis - PubMed In summary, though having some functional overlapping with the gut microbiota of herbivorous and omnivorous hosts, the FGI microbiota differentially codify functions in pathways related to lignocellulose breakdown, detoxification of plant secondary metabolites, metabolism of simple sugars, fungal cell wall deconstruction, biofilm formation, antimicrobials biosynthesis, and diverse nutrient cycling routes (Fig. Front. 8.14: Symbiotic Relationships of Fungi - Biology LibreTexts Defense contracts: molecular protection in insect-microbe symbioses. ifkov, L. et al. Article Annu. Rabeling, C., Verhaagh, M. & Engels, W. Comparative study of nest architecture and colony structure of the fungus-growing ants, Mycocepurus goeldii and M. smithii. Evolutionary History of the Symbiosis Between Fungus-Growing Ants and M. goeldii microbiota sits close to this cluster, though presenting Pseudomonas, Dysgonomonas, Pantoea, and Enterobacter as the most abundant genera. Two general patterns were observed for the taxonomically assigned CAZy sequences of gut microbiota of omnivorous vertebrates (Fig. Brune, A., Miambi, E. & Breznak, J. Syst. Proc. Quality-controlled reads were assembled using default settings in MEGAHIT v1.0.692. Microbiol. Soil Biol. Boone, C. K. Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. 37, 699735. Engel, P., Martinson, V. G. & Moran, N. A. Functional diversity within the simple gut microbiota of the honey bee. Environ. https://doi.org/10.1073/pnas.1202970109 (2012). https://doi.org/10.1128/AEM.03833-12 (2013). Google Scholar. Comparisons between host groups were determined using the Whites test105 (c) Most abundant GH (glycoside hydrolases). Markowitz, V. M. et al. We are grateful to Dr. Luiz C. Forti for helping with field sampling and to Dr. Srgio Kakazu for helping with DNA purification. (a) UPGMA-clustering estimated based on BrayCurtis distances (Boot N=10,000). Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol. 79, 37703778. Being associated with functionally herbivorous hosts suggests that these bacterial communities could take part in lignocellulose breakdown. 193, 28902891. Aphid and Ants exhibit symbiosis mBio 5, e02077-14. J. Chem. Berasategui, A. et al. We empirically verified this adaptation resulting in DNA samples with higher quantity and quality from our bacterial samples. sexdens rubropilosa gardens follows the general taxonomic composition pattern found in other FGI, i.e., dominated by Gammaproteobacteria. M.B. Fungiculture environments are also associated with a bacterial community that potentially regulates the symbiosis. Brabcov, V., tursov, M. & Baldrian, P. Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. sexdens rubropilosa.
